Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 May;179(10):3085–3094. doi: 10.1128/jb.179.10.3085-3094.1997

Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria.

P J Christie 1
PMCID: PMC179082  PMID: 9150199

Full Text

The Full Text of this article is available as a PDF (186.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson L. B., Hertzel A. V., Das A. Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):8889–8894. doi: 10.1073/pnas.93.17.8889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balzer D., Pansegrau W., Lanka E. Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative transfer of plasmid RP4. J Bacteriol. 1994 Jul;176(14):4285–4295. doi: 10.1128/jb.176.14.4285-4295.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bardwell J. C. Building bridges: disulphide bond formation in the cell. Mol Microbiol. 1994 Oct;14(2):199–205. doi: 10.1111/j.1365-2958.1994.tb01281.x. [DOI] [PubMed] [Google Scholar]
  4. Baron C., Llosa M., Zhou S., Zambryski P. C. VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1. J Bacteriol. 1997 Feb;179(4):1203–1210. doi: 10.1128/jb.179.4.1203-1210.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baron C., Thorstenson Y. R., Zambryski P. C. The lipoprotein VirB7 interacts with VirB9 in the membranes of Agrobacterium tumefaciens. J Bacteriol. 1997 Feb;179(4):1211–1218. doi: 10.1128/jb.179.4.1211-1218.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bayer M., Eferl R., Zellnig G., Teferle K., Dijkstra A., Koraimann G., Högenauer G. Gene 19 of plasmid R1 is required for both efficient conjugative DNA transfer and bacteriophage R17 infection. J Bacteriol. 1995 Aug;177(15):4279–4288. doi: 10.1128/jb.177.15.4279-4288.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beaupré C. E., Bohne J., Dale E. M., Binns A. N. Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J Bacteriol. 1997 Jan;179(1):78–89. doi: 10.1128/jb.179.1.78-89.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Beijersbergen A., Dulk-Ras A. D., Schilperoort R. A., Hooykaas P. J. Conjugative Transfer by the Virulence System of Agrobacterium tumefaciens. Science. 1992 May 29;256(5061):1324–1327. doi: 10.1126/science.256.5061.1324. [DOI] [PubMed] [Google Scholar]
  9. Beijersbergen A., Smith S. J., Hooykaas P. J. Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid. 1994 Sep;32(2):212–218. doi: 10.1006/plas.1994.1057. [DOI] [PubMed] [Google Scholar]
  10. Berger B. R., Christie P. J. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J Bacteriol. 1994 Jun;176(12):3646–3660. doi: 10.1128/jb.176.12.3646-3660.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Berger B. R., Christie P. J. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J Bacteriol. 1993 Mar;175(6):1723–1734. doi: 10.1128/jb.175.6.1723-1734.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Binns A. N., Beaupré C. E., Dale E. M. Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010. J Bacteriol. 1995 Sep;177(17):4890–4899. doi: 10.1128/jb.177.17.4890-4899.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bundock P., Hooykaas P. J. Integration of Agrobacterium tumefaciens T-DNA in the Saccharomyces cerevisiae genome by illegitimate recombination. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15272–15275. doi: 10.1073/pnas.93.26.15272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bundock P., den Dulk-Ras A., Beijersbergen A., Hooykaas P. J. Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J. 1995 Jul 3;14(13):3206–3214. doi: 10.1002/j.1460-2075.1995.tb07323.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Censini S., Lange C., Xiang Z., Crabtree J. E., Ghiara P., Borodovsky M., Rappuoli R., Covacci A. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14648–14653. doi: 10.1073/pnas.93.25.14648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Christie P. J., Ward J. E., Jr, Gordon M. P., Nester E. W. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9677–9681. doi: 10.1073/pnas.86.24.9677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Christie P. J., Ward J. E., Winans S. C., Nester E. W. The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J Bacteriol. 1988 Jun;170(6):2659–2667. doi: 10.1128/jb.170.6.2659-2667.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Citovsky V., DE Vos G., Zambryski P. Single-Stranded DNA Binding Protein Encoded by the virE Locus of Agrobacterium tumefaciens. Science. 1988 Apr 22;240(4851):501–504. doi: 10.1126/science.240.4851.501. [DOI] [PubMed] [Google Scholar]
  19. Citovsky V., Zupan J., Warnick D., Zambryski P. Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science. 1992 Jun 26;256(5065):1802–1805. doi: 10.1126/science.1615325. [DOI] [PubMed] [Google Scholar]
  20. Covacci A., Rappuoli R. Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol. 1993 May;8(3):429–434. doi: 10.1111/j.1365-2958.1993.tb01587.x. [DOI] [PubMed] [Google Scholar]
  21. Dale E. M., Binns A. N., Ward J. E., Jr Construction and characterization of Tn5virB, a transposon that generates nonpolar mutations, and its use to define virB8 as an essential virulence gene in Agrobacterium tumefaciens. J Bacteriol. 1993 Feb;175(3):887–891. doi: 10.1128/jb.175.3.887-891.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Dang T. A., Christie P. J. The VirB4 ATPase of Agrobacterium tumefaciens is a cytoplasmic membrane protein exposed at the periplasmic surface. J Bacteriol. 1997 Jan;179(2):453–462. doi: 10.1128/jb.179.2.453-462.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Das A. Agrobacterium tumefaciens virE operon encodes a single-stranded DNA-binding protein. Proc Natl Acad Sci U S A. 1988 May;85(9):2909–2913. doi: 10.1073/pnas.85.9.2909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dijkstra A. J., Keck W. Peptidoglycan as a barrier to transenvelope transport. J Bacteriol. 1996 Oct;178(19):5555–5562. doi: 10.1128/jb.178.19.5555-5562.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Farizo K. M., Cafarella T. G., Burns D. L. Evidence for a ninth gene, ptlI, in the locus encoding the pertussis toxin secretion system of Bordetella pertussis and formation of a PtlI-PtlF complex. J Biol Chem. 1996 Dec 6;271(49):31643–31649. doi: 10.1074/jbc.271.49.31643. [DOI] [PubMed] [Google Scholar]
  26. Fath M. J., Kolter R. ABC transporters: bacterial exporters. Microbiol Rev. 1993 Dec;57(4):995–1017. doi: 10.1128/mr.57.4.995-1017.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Fernandez D., Dang T. A., Spudich G. M., Zhou X. R., Berger B. R., Christie P. J. The Agrobacterium tumefaciens virB7 gene product, a proposed component of the T-complex transport apparatus, is a membrane-associated lipoprotein exposed at the periplasmic surface. J Bacteriol. 1996 Jun;178(11):3156–3167. doi: 10.1128/jb.178.11.3156-3167.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Fernandez D., Spudich G. M., Zhou X. R., Christie P. J. The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol. 1996 Jun;178(11):3168–3176. doi: 10.1128/jb.178.11.3168-3176.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Finberg K. E., Muth T. R., Young S. P., Maken J. B., Heitritter S. M., Binns A. N., Banta L. M. Interactions of VirB9, -10, and -11 with the membrane fraction of Agrobacterium tumefaciens: solubility studies provide evidence for tight associations. J Bacteriol. 1995 Sep;177(17):4881–4889. doi: 10.1128/jb.177.17.4881-4889.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Fullner K. J., Lara J. C., Nester E. W. Pilus assembly by Agrobacterium T-DNA transfer genes. Science. 1996 Aug 23;273(5278):1107–1109. doi: 10.1126/science.273.5278.1107. [DOI] [PubMed] [Google Scholar]
  31. Fullner K. J., Nester E. W. Temperature affects the T-DNA transfer machinery of Agrobacterium tumefaciens. J Bacteriol. 1996 Mar;178(6):1498–1504. doi: 10.1128/jb.178.6.1498-1504.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Fullner K. J., Stephens K. M., Nester E. W. An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA. Mol Gen Genet. 1994 Dec 15;245(6):704–715. doi: 10.1007/BF00297277. [DOI] [PubMed] [Google Scholar]
  33. Fuqua C., Winans S. C., Greenberg E. P. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol. 1996;50:727–751. doi: 10.1146/annurev.micro.50.1.727. [DOI] [PubMed] [Google Scholar]
  34. Galán J. E. Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol. 1996 Apr;20(2):263–271. doi: 10.1111/j.1365-2958.1996.tb02615.x. [DOI] [PubMed] [Google Scholar]
  35. Guralnick B., Thomsen G., Citovsky V. Transport of DNA into the nuclei of xenopus oocytes by a modified VirE2 protein of Agrobacterium. Plant Cell. 1996 Mar;8(3):363–373. doi: 10.1105/tpc.8.3.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Haase J., Lurz R., Grahn A. M., Bamford D. H., Lanka E. Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific phage propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J Bacteriol. 1995 Aug;177(16):4779–4791. doi: 10.1128/jb.177.16.4779-4791.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hardie K. R., Lory S., Pugsley A. P. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 1996 Mar 1;15(5):978–988. [PMC free article] [PubMed] [Google Scholar]
  38. Heinemann J. A., Sprague G. F., Jr Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature. 1989 Jul 20;340(6230):205–209. doi: 10.1038/340205a0. [DOI] [PubMed] [Google Scholar]
  39. Hobbs M., Mattick J. S. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol. 1993 Oct;10(2):233–243. doi: 10.1111/j.1365-2958.1993.tb01949.x. [DOI] [PubMed] [Google Scholar]
  40. Jones A. L., Lai E. M., Shirasu K., Kado C. I. VirB2 is a processed pilin-like protein encoded by the Agrobacterium tumefaciens Ti plasmid. J Bacteriol. 1996 Oct;178(19):5706–5711. doi: 10.1128/jb.178.19.5706-5711.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Jones A. L., Shirasu K., Kado C. I. The product of the virB4 gene of Agrobacterium tumefaciens promotes accumulation of VirB3 protein. J Bacteriol. 1994 Sep;176(17):5255–5261. doi: 10.1128/jb.176.17.5255-5261.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kado C. I. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis. Mol Microbiol. 1994 Apr;12(1):17–22. doi: 10.1111/j.1365-2958.1994.tb00990.x. [DOI] [PubMed] [Google Scholar]
  43. Kuldau G. A., De Vos G., Owen J., McCaffrey G., Zambryski P. The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol Gen Genet. 1990 Apr;221(2):256–266. doi: 10.1007/BF00261729. [DOI] [PubMed] [Google Scholar]
  44. Lessl M., Balzer D., Pansegrau W., Lanka E. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J Biol Chem. 1992 Oct 5;267(28):20471–20480. [PubMed] [Google Scholar]
  45. Lessl M., Lanka E. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell. 1994 May 6;77(3):321–324. doi: 10.1016/0092-8674(94)90146-5. [DOI] [PubMed] [Google Scholar]
  46. Lin T. S., Kado C. I. The virD4 gene is required for virulence while virD3 and orf5 are not required for virulence of Agrobacterium tumefaciens. Mol Microbiol. 1993 Aug;9(4):803–812. doi: 10.1111/j.1365-2958.1993.tb01739.x. [DOI] [PubMed] [Google Scholar]
  47. Macnab R. M. Genetics and biogenesis of bacterial flagella. Annu Rev Genet. 1992;26:131–158. doi: 10.1146/annurev.ge.26.120192.001023. [DOI] [PubMed] [Google Scholar]
  48. Miranda A., Janssen G., Hodges L., Peralta E. G., Ream W. Agrobacterium tumefaciens transfers extremely long T-DNAs by a unidirectional mechanism. J Bacteriol. 1992 Apr;174(7):2288–2297. doi: 10.1128/jb.174.7.2288-2297.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mushegian A. R., Fullner K. J., Koonin E. V., Nester E. W. A family of lysozyme-like virulence factors in bacterial pathogens of plants and animals. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7321–7326. doi: 10.1073/pnas.93.14.7321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Okamoto S., Toyoda-Yamamoto A., Ito K., Takebe I., Machida Y. Localization and orientation of the VirD4 protein of Agrobacterium tumefaciens in the cell membrane. Mol Gen Genet. 1991 Aug;228(1-2):24–32. doi: 10.1007/BF00282443. [DOI] [PubMed] [Google Scholar]
  51. Pansegrau W., Lanka E., Barth P. T., Figurski D. H., Guiney D. G., Haas D., Helinski D. R., Schwab H., Stanisich V. A., Thomas C. M. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J Mol Biol. 1994 Jun 24;239(5):623–663. doi: 10.1006/jmbi.1994.1404. [DOI] [PubMed] [Google Scholar]
  52. Pansegrau W., Schoumacher F., Hohn B., Lanka E. Site-specific cleavage and joining of single-stranded DNA by VirD2 protein of Agrobacterium tumefaciens Ti plasmids: analogy to bacterial conjugation. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11538–11542. doi: 10.1073/pnas.90.24.11538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pansegrau W., Schröder W., Lanka E. Concerted action of three distinct domains in the DNA cleaving-joining reaction catalyzed by relaxase (TraI) of conjugative plasmid RP4. J Biol Chem. 1994 Jan 28;269(4):2782–2789. [PubMed] [Google Scholar]
  54. Pansegrau W., Schröder W., Lanka E. Relaxase (TraI) of IncP alpha plasmid RP4 catalyzes a site-specific cleaving-joining reaction of single-stranded DNA. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2925–2929. doi: 10.1073/pnas.90.7.2925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Parsot C., Ménard R., Gounon P., Sansonetti P. J. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol. 1995 Apr;16(2):291–300. doi: 10.1111/j.1365-2958.1995.tb02301.x. [DOI] [PubMed] [Google Scholar]
  56. Piers K. L., Heath J. D., Liang X., Stephens K. M., Nester E. W. Agrobacterium tumefaciens-mediated transformation of yeast. Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1613–1618. doi: 10.1073/pnas.93.4.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pizza M., Bugnoli M., Manetti R., Covacci A., Rappuoli R. The subunit S1 is important for pertussis toxin secretion. J Biol Chem. 1990 Oct 15;265(29):17759–17763. [PubMed] [Google Scholar]
  58. Pohlman R. F., Genetti H. D., Winans S. C. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol Microbiol. 1994 Nov;14(4):655–668. doi: 10.1111/j.1365-2958.1994.tb01304.x. [DOI] [PubMed] [Google Scholar]
  59. Pugsley A. P. The complete general secretory pathway in gram-negative bacteria. Microbiol Rev. 1993 Mar;57(1):50–108. doi: 10.1128/mr.57.1.50-108.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rashkova S., Spudich G. M., Christie P. J. Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J Bacteriol. 1997 Feb;179(3):583–591. doi: 10.1128/jb.179.3.583-591.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Regensburg-Tuïnk A. J., Hooykaas P. J. Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature. 1993 May 6;363(6424):69–71. doi: 10.1038/363069a0. [DOI] [PubMed] [Google Scholar]
  62. Rossi L., Hohn B., Tinland B. Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):126–130. doi: 10.1073/pnas.93.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sandkvist M., Bagdasarian M., Howard S. P., DiRita V. J. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J. 1995 Apr 18;14(8):1664–1673. doi: 10.1002/j.1460-2075.1995.tb07155.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Scheiffele P., Pansegrau W., Lanka E. Initiation of Agrobacterium tumefaciens T-DNA processing. Purified proteins VirD1 and VirD2 catalyze site- and strand-specific cleavage of superhelical T-border DNA in vitro. J Biol Chem. 1995 Jan 20;270(3):1269–1276. doi: 10.1074/jbc.270.3.1269. [DOI] [PubMed] [Google Scholar]
  65. Shirasu K., Kado C. I. Membrane location of the Ti plasmid VirB proteins involved in the biosynthesis of a pilin-like conjugative structure on Agrobacterium tumefaciens. FEMS Microbiol Lett. 1993 Aug 1;111(2-3):287–294. doi: 10.1111/j.1574-6968.1993.tb06400.x. [DOI] [PubMed] [Google Scholar]
  66. Shirasu K., Kado C. I. The virB operon of the Agrobacterium tumefaciens virulence regulon has sequence similarities to B, C and D open reading frames downstream of the pertussis toxin-operon and to the DNA transfer-operons of broad-host-range conjugative plasmids. Nucleic Acids Res. 1993 Jan 25;21(2):353–354. doi: 10.1093/nar/21.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Shirasu K., Koukolíková-Nicola Z., Hohn B., Kado C. I. An inner-membrane-associated virulence protein essential for T-DNA transfer from Agrobacterium tumefaciens to plants exhibits ATPase activity and similarities to conjugative transfer genes. Mol Microbiol. 1994 Feb;11(3):581–588. doi: 10.1111/j.1365-2958.1994.tb00338.x. [DOI] [PubMed] [Google Scholar]
  68. Shirasu K., Morel P., Kado C. I. Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis. Mol Microbiol. 1990 Jul;4(7):1153–1163. doi: 10.1111/j.1365-2958.1990.tb00690.x. [DOI] [PubMed] [Google Scholar]
  69. Spudich G. M., Fernandez D., Zhou X. R., Christie P. J. Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7512–7517. doi: 10.1073/pnas.93.15.7512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Stephens K. M., Roush C., Nester E. Agrobacterium tumefaciens VirB11 protein requires a consensus nucleotide-binding site for function in virulence. J Bacteriol. 1995 Jan;177(1):27–36. doi: 10.1128/jb.177.1.27-36.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Sundberg C., Meek L., Carroll K., Das A., Ream W. VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J Bacteriol. 1996 Feb;178(4):1207–1212. doi: 10.1128/jb.178.4.1207-1212.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Thompson D. V., Melchers L. S., Idler K. B., Schilperoort R. A., Hooykaas P. J. Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon. Nucleic Acids Res. 1988 May 25;16(10):4621–4636. doi: 10.1093/nar/16.10.4621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Thorstenson Y. R., Kuldau G. A., Zambryski P. C. Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J Bacteriol. 1993 Aug;175(16):5233–5241. doi: 10.1128/jb.175.16.5233-5241.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Thorstenson Y. R., Zambryski P. C. The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens. J Bacteriol. 1994 Mar;176(6):1711–1717. doi: 10.1128/jb.176.6.1711-1717.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Tinland B., Hohn B., Puchta H. Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8000–8004. doi: 10.1073/pnas.91.17.8000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tinland B., Schoumacher F., Gloeckler V., Bravo-Angel A. M., Hohn B. The Agrobacterium tumefaciens virulence D2 protein is responsible for precise integration of T-DNA into the plant genome. EMBO J. 1995 Jul 17;14(14):3585–3595. doi: 10.1002/j.1460-2075.1995.tb07364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tummuru M. K., Sharma S. A., Blaser M. J. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells. Mol Microbiol. 1995 Dec;18(5):867–876. doi: 10.1111/j.1365-2958.1995.18050867.x. [DOI] [PubMed] [Google Scholar]
  78. Vogel A. M., Das A. Mutational analysis of Agrobacterium tumefaciens virD2: tyrosine 29 is essential for endonuclease activity. J Bacteriol. 1992 Jan;174(1):303–308. doi: 10.1128/jb.174.1.303-308.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Ward J. E., Akiyoshi D. E., Regier D., Datta A., Gordon M. P., Nester E. W. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem. 1988 Apr 25;263(12):5804–5814. [PubMed] [Google Scholar]
  80. Ward J. E., Akiyoshi D. E., Regier D., Datta A., Gordon M. P., Nester E. W. Correction: characterization of the virB operon from Agrobacterium tumefaciens Ti plasmid. J Biol Chem. 1990 Mar 15;265(8):4768–4768. [PubMed] [Google Scholar]
  81. Ward J. E., Jr, Dale E. M., Binns A. N. Activity of the Agrobacterium T-DNA transfer machinery is affected by virB gene products. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9350–9354. doi: 10.1073/pnas.88.20.9350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Ward J. E., Jr, Dale E. M., Christie P. J., Nester E. W., Binns A. N. Complementation analysis of Agrobacterium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virB10, and virB11 are essential virulence genes. J Bacteriol. 1990 Sep;172(9):5187–5199. doi: 10.1128/jb.172.9.5187-5199.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Ward J. E., Jr, Dale E. M., Nester E. W., Binns A. N. Identification of a virB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens. J Bacteriol. 1990 Sep;172(9):5200–5210. doi: 10.1128/jb.172.9.5200-5210.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Waters V. L., Guiney D. G. Processes at the nick region link conjugation, T-DNA transfer and rolling circle replication. Mol Microbiol. 1993 Sep;9(6):1123–1130. doi: 10.1111/j.1365-2958.1993.tb01242.x. [DOI] [PubMed] [Google Scholar]
  85. Weiss A. A., Johnson F. D., Burns D. L. Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2970–2974. doi: 10.1073/pnas.90.7.2970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Winans S. C., Burns D. L., Christie P. J. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 1996 Feb;4(2):64–68. doi: 10.1016/0966-842X(96)81513-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Winans S. C. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol Rev. 1992 Mar;56(1):12–31. doi: 10.1128/mr.56.1.12-31.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Yusibov V. M., Steck T. R., Gupta V., Gelvin S. B. Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2994–2998. doi: 10.1073/pnas.91.8.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Zupan J. R., Zambryski P. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 1995 Apr;107(4):1041–1047. doi: 10.1104/pp.107.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES